Migraine COG

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Migraine and cognitive function

A life-course study

Karen E. Waldie, PhD; Markus Hausmann, PhD; Barry J. Milne, MSc; andRichie Poulton, DipClinPsyc, PhD

Abstract—Objective: To investigate the association between migraine and cognitive ability among members of a longitu-

dinal birth cohort study. Methods: Headache status was determined at age 26 (migraine, tension-type headache [TTH],

headache-free control subjects) according to International Headache Society criteria, and data relating to cognitive and

academic performance from ages 3 to 26 years were analyzed. Results: Study members diagnosed with migraine were

subtly but significantly impaired, compared with those with TTH and headache-free control subjects, on tests of verbal

ability (especially language reception) from ages 3 to 13, independent of headache history. Performance on other tasks,

including reading, arithmetic, motor, and spatial ability, was normal. The association between migraine and verbal

functioning also appeared to impact on later academic success. Conclusion: Findings suggest that the poorer verbal

performance was unlikely to have resulted from cumulative attacks and may be due to developmental factors beginning in

utero.

NEUROLOGY 2002;59:904–908

Individuals who experience migraine appear to pro-cess auditory and visual information differently fromthose without migraine. Functional and electrophysi-ologic alterations in cortical functioning have beenfound during the migraine interval,1-5 which may beassociated with cognitive impairment as demon-strated on tests of perception,6,7 psychomotor ability,8

attention,9-11 and verbal memory.12,13 However, notall studies have found such cortical alterations14 orcognitive performance decrements.15,16 Thus, it re-mains unclear whether migraine is associated withcognitive efficiency and, if so, to what degree and

specificity.The inconsistency in the migraine literature

might be a result of methodologic limitations. Forexample, studies have generally relied upon subjectswho have been referred to neurologists or specialistheadache clinics, resulting in a highly unrepresenta-tive sample.17 Moreover, few studies have used ade-quate comparison groups, and many are oftenconstrained by the use of cross-sectional designs. Itis generally preferable to employ longitudinal de-signs, where changes in the cognitive performance of migraineurs can be compared with corresponding changes in control subjects throughout development.

We investigated the association between mi-graine, tension-type headache (TTH) (diagnosed ac-cording to International Headache Society [IHS]criteria),18 and cognitive performance among mem-bers of a representative cohort study over a period of

23 years. If the putative poorer cognitive perfor-mance of migraineurs is a consequence of the cumu-lative effects of headache attacks and thus a result of repeated vascular insult,19,20 cognitive deficits shouldbe first detectable later in life, and individuals witha childhood history of headache should perform morepoorly than those with no history. Alternatively, if there were evidence of cognitive impairment that isspecific to migraineurs from an early age, it wouldsuggest that migraine is associated with atypicalneurodevelopment in utero or infancy.

Methods. Participants and general procedure. Thesample comprised members of the Dunedin Multidisci-

plinary Health and Development Study.21 This is a longitu-

dinal investigation of the health and behavior of a

complete cohort of individuals born in Dunedin, New Zea-

land, between 1 April 1972 and 31 March 1973. Study

members have been assessed individually on a wide vari-

ety of psychological and medical measures at ages 3, 5, 7,

9, 11, 13, 15, 18, 21, and most recently in 1998 and 1999 at

age 26 (n ϭ 980; 96.2% of the living cohort).

Primary headache diagnosis. As previously document-

ed,22,23 at the age 26 assessment, a registered nurse or

medical practitioner asked 979 study members a series of

questions concerning headache pain characteristics and

symptoms in the last year (abstracted from the IHS classi-fication). Almost 12% fulfilled IHS criteria for migraine

(n ϭ 114), and 11.1% were diagnosed with TTH (n ϭ 109).

Migraine was 3.5 times more frequent among women than

men (95% CI 2.3 to 5.4), and TTH was 2.3 times more

From the Department of Psychology (Drs. Waldie and Hausmann), University of Auckland; and Dunedin Multidisciplinary Health and Development

Research Unit (Dr. Poulton and B.J. Milne), Department of Preventive and Social Medicine, Dunedin School of Medicine, University of Otago, Dunedin, New

Zealand.

The Dunedin Multidisciplinary Health and Development Research Unit is supported by the Health Research Council of New Zealand. Data collection was

partially supported by a National Heart Foundation Grant of New Zealand and US NIMH grant MH45070.

Received March 22, 2002. Accepted in final form June 11, 2002.

Address correspondence and reprint requests to Dr. Karen E. Waldie, Department of Psychology, University of Auckland, Private Bag 92101 Auckland, New

Zealand; e-mail: [email protected]

904 Copyright © 2002 by AAN Enterprises, Inc.



frequent among women (95% CI 1.5 to 3.4). Study mem-

bers who reported headaches were excluded from analyses

if they did not meet IHS criteria or if medical records

indicated their headaches were likely due to head trauma.

Almost half (48%) of the migraineurs were taking at

least one form of prescription medication during the last

12 months compared with 35% of control subjects and 55%

of individuals with TTH. Only 3% of migraineurs were

taking migraine medication.

To assess whether childhood headaches influenced cog-nitive performance, possibly owing to impaired concentra-

tion or school absence, study members were grouped

according to whether headaches occurred during childhood

(ages 7, 9, 11, or 13 years measured with the Rutter Child

Scale A)24 or later. There were no sex differences in those

reporting childhood headache (54.1% boys).

Family socioeconomic status. Family socioeconomic

status (SES) was measured on a 6-point scale25 and ana-

lyzed as the average of the highest SES level of either

parent at the study member’s birth through to age 15.

Study members were designated as growing up in families

whose mean SES was low (Groups 6 and 5; e.g., oyster

canner, car painter; n ϭ 215, 21%), medium (Groups 4 and

3; e.g., butcher, secretary; n ϭ 649, 63%), or high (Groups 2and 1; e.g., architect, dentist; n ϭ 167, 16%).

Maternal headache. At the age 26 assessment, study

members’ biologic mothers were asked if they had frequent

headaches. Headache information was also available for

mothers who accompanied their child to the age 5, 7, and 9

assessments and completed the Rutter Malaise Inventory

B.24 One hundred sixty-eight mothers (18.4%) were classi-

fied as having a history of headache based on a positive

response during the age 26 assessment and at least one of

the earlier assessments.

Cognitive and neuropsychological measures. The Pea-

body Picture Vocabulary Test (PPVT)26 was administered

at age 3 to assess receptive language ability and the Ver-

bal Comprehension and Verbal Expression subscales of the

Illinois Test of Psycholinguistic Ability (ITPA)27 were ad-

ministered at ages 7 and 9. The Wechsler Intelligence

Scale for Children–Revised28 was administered (omitting

Comprehension and Picture Arrangement subtests) at

ages 7, 9, 11, and 13. The Burt Word Reading Test (1974

revision)29 was administered at ages 7, 9, 11, 13, 15, and

18. At age 11, a trained audiometrist tested pure tone

thresholds; a speech-in-noise (SPIN) test that was devel-

oped by the audiometrist for use in New Zealand was ad-

ministered at ages 11 and 13.

Hand preference30 was determined at age 7, and infor-

mation about the handedness of first-degree relatives was

obtained from 563 study members at age 26 (58% of con-trols, 53% migraine, 62% TTH). Migraineurs were more

likely to be mixed or left handed relative to control subjects

(2 ϭ 3.2, p ϭ 0.049) and to be slightly more likely than

control subjects to have at least one left-handed relative

(10% versus 7%).

Schoo l achievement and qual ifications. Academic

achievement was estimated from the total scores on New

Zealand national exams and a standardized grading system

during the final 2 years of high school (ages 15 to 17). Scores

from the School Certificate Examinations ranged between 6

and 42 (mean ϭ 22.0, SD ϭ 7.4), and Sixth Form Certificate

scores were based on sums of grades across up to six subjects

(ranging between 6 and 54; mean ϭ 26.0, SD ϭ 10.1). At the

age 26 assessment, information was obtained about

postschool academic qualifications.

Data analysis. Repeated measures analyses of vari-

ance were performed on data obtained on more than one

occasion. 2 and logistic regression analyses (odds ratios

[OR] with 95% CI) were conducted for categorical mea-

sures. Sex, family SES, prescription drug use, and child-hood history of headache were included as independent

variables where sample size permitted. In preliminary

analyses (data not shown), analyses of covariance were

performed to ensure that effects reported below were not

due to maternal history of headache, anxiety, or depressive

disorder.

Results. The psychological and medical measures that

were used in the following analyses are presented in the

table. A repeated measures analysis of variance revealed

that verbal IQ (F[6,2145] ϭ 0.74, p ϭ 0.62) and perfor-

mance IQ (F[6,2142] ϭ 1.2, p ϭ 0.29) did not differ across

Table Measures and age of assessment used in this study to

determine medical, cognitive, and academic functioning of

members of the Dunedin longitudinal cohort study

Measures Assessment age, y

Medical investigation

Primary headache diagnosis (IHS) 26

Headache complaints (Rutter Child Scale A) 7, 9, 11, 13

Sensory functions Auditory reception and discrimination (SPIN)* 11, 13

Peripheral hearing (pure tone threshold) 11

Cognitive/neuropsychological measures

Peabody Picture Vocabulary Test 3

Verbal IQ (WISC-R) 7, 9, 11, 13

Performance IQ (WISC-R) 7, 9, 11, 13

Burt Word Reading Test 7, 9, 11, 13, 15, 18

Verbal Comprehension (ITPA) 7, 9

Verbal Expression (ITPA) 7, 9

Hand Preference (HTLD/self-report) 7, 26

School achievement

Certificate E xamination (English/Math) 15–16

Sixth Form Certificate grades 16–17

Academic qualification 26

Family variables

Famil y socioeconomic status Birth, 3, 5, 7, 9, 11, 13, 15

Maternal history of headache 5, 7, 9, 26

Sample size fluctuates across various measures because of missing data.

* Study members were asked to repeat word lists (scored phonemically)

that were presented orally at 60 dB sound pressure level above the

child’s pure tone threshold at 1 kHz in 1) two no-noise conditions, 2) two

noise conditions with signal-to-noise ratios of 5 dB, and 3) two noise con-

ditions with signal-to-noise ratios of 10 dB.

IHS ϭ International Headache Society; SPIN ϭ speech in noise; WISC-R ϭ

Wechsler Intelligence Scale for Children–Revised; ITPA ϭ Illinois Test of

Psycholinguistic Ability; HTLD ϭ Harris Tests of Lateral Dominance.

September (2 of 2) 2002 NEUROLOGY 59 905



assessment age as a function of headache group (migraine,

TTH, control subjects).

The main effect of group was significant only for verbal

IQ, with migraineurs showing lower verbal IQ scores

(mean ϭ 100.6 Ϯ 11.4) than both control subjects (mean ϭ

105.7 Ϯ 13.5; p ϭ 0.019) and those with TTH (mean ϭ

104.4 Ϯ 13.8; p ϭ 0.036). Figure 1 shows the mean verbal

IQ scores for each headache group across the four assess-

ment ages. Separate analyses revealed no sex differences

in verbal IQ according to headache group; nor was there an

effect of prescription drug use or a drug-use-by-group in-

teraction (all p Ͼ 0.50).

To test the hypothesis that migraineurs with a historyof childhood headache might be at increased risk for cogni-

tive impairment due to missed educational opportunities,

repeated measures analysis of variance was conducted on

the verbal IQ scores. Mean scores at each assessment age

for each headache group by childhood history and head-

ache combination are presented in figure 2. The analysis

showed a significant main effect of age (F[3,2106] ϭ 11.3,

p Ͻ 0.001), an age-by-headache-history interaction

(F[3,2106] ϭ 6.1, p Ͻ 0.001), and an age-by-headache-

history-by-group interaction (F[6,2106] ϭ 3.0, p ϭ 0.006).

Analysis of simple effects by headache group at each

assessment age (i.e., ages 7, 9, 11, and 13) revealed that

those who had childhood headache scored consistently

more poorly than those without a history on verbal IQ.

However, this effect was restricted to those later diagnosed

with TTH (all p Ͻ 0.04) and to those whose headaches did

not persist (all p Ͻ 0.03). Among those with childhood

headache, only 17% were later diagnosed with migraineand 9% with TTH. Importantly, migraineurs with child-

hood headache did not perform more poorly than control

subjects at any assessment age.

A separate analysis with performance IQ (across the

four assessment ages) did not reveal any main or interac-

tion effects with childhood history of headache (history:

106.6 Ϯ 12.6; no history: 110.5 Ϯ 12.6).

With regard to family SES, study members with child-

hood headache (23.7%) were more likely to have come from

low SES families than those without headache (17.9%)

(2 ϭ 6.15, p ϭ 0.046). In contrast, those who were diag-

nosed with migraine or TTH in adulthood did not differ

from each other or from headache-free control subjects on

family SES.Timing of cognitive changes. Receptive language was

measured at age 3 with the PPVT, which was strongly

correlated with mean verbal IQ in this sample (r ϭ 0.56,

p Ͻ 0.001). Analysis of variance, with headache group and

sex as independent measures, was used to test whether

the poorer verbal performance in migraineurs occurred

prior to the onset of headache symptoms. There was a

significant main effect of group (F[2,902] ϭ 3.4, p ϭ 0.032),

with those with migraine at age 26 (mean ϭ 21.6 Ϯ 9.2)

performing more poorly than those with TTH (mean ϭ

24.9 Ϯ 8.9) and headache-free control subjects (mean ϭ

23.8 Ϯ 9.6). The main effects of sex and the group-by-sex

interaction were not significant.Global verbal deficit versus specific language difficulty.

Considering that verbal IQ comprises different components

of language functioning, we separately analyzed the Wech-

sler Intelligence Scale for Children–Revised subscales (i.e.,

information, similarities, arithmetic, vocabulary). Individ-

ual repeated measures analysis revealed that the head-

ache groups differed at each testing age on the information

(F[2,761] ϭ 4.2, p ϭ 0.015), similarities (F[2,701] ϭ 6.1,

Figure 1. The mean verbal IQ scores at ages 7, 9, 11, and

13 of study members who were diagnosed at age 26 with

migraine (n ϭ 114) ( ), tension-type headache (TTH; nϭ

109) ( f ), or no headache ( ‘ )(n ϭ 739).

Figure 2. The mean verbal IQ scores, across four childhood assessment ages, of study members diagnosed in adulthood

with migraine (n ϭ 114), tension-type headache (TTH; n ϭ 109), or no headache (n ϭ 739) as a function of childhood

history of headache (solid line) or no history of headache (dotted line). Significant group differences are indicated (*p Ͻ

0.05). WISC-R ϭ Wechsler Intelligence Scale for Children – Revised.

906 NEUROLOGY 59 September (2 of 2) 2002



p ϭ 0.002), and vocabulary (F[2,679] ϭ 4.9, p ϭ 0.007)

subscales but not the arithmetic subscale (F[2,699] ϭ 2.9,

p ϭ 0.067). Post hoc Bonferroni tests showed that mi-

graineurs performed significantly more poorly on each

measure than control subjects. They also had lower scores

on the information ( p ϭ 0.09) and vocabulary ( p ϭ 0.056)

subscales than those with TTH, but only the similarities

subscale was significantly lower.

Reading, verbal expression, and reception. Analysis of

variance, with reading scores from the age 7, 9, 11, 13, 15,and 18 assessments as repeated measures, showed that

reading performance did not change across time according

to headache group (F[10,3485] ϭ 1.3, p ϭ 0.20). Interest-

ingly, the reading ability of migraineurs was slightly bet-

ter (mean ϭ 72.6 Ϯ 15.4) than that of control subjects

(means ϭ 70.9 Ϯ 17.0) and those with TTH (mean ϭ

70.6 Ϯ 15.8), but the main effect of group was not signifi-

cant. Similarly, verbal expression measured with the ITPA

was not different between headache groups (F[2,826] ϭ

0.2, p ϭ 0.85).

In contrast, group differences on the measure of verbal

comprehension at the same ages (F[2,837] ϭ 3.1, p ϭ

0.049) showed that those with migraine performed more

poorly than control subjects ( p ϭ 0.024). Migraineurs alsoperformed more poorly on the SPIN tests when the signal-

to-noise ratio was at 10 dB (F[1,473] ϭ 3.9, p ϭ 0.048) but

not at 5 dB signal-to-noise ratio or in the no-noise condi-

tion. There were no differences between groups on tests of

pure tone audiometry thresholds (peripheral hearing).

Later academic performance. Study members with mi-

graine (mean ϭ 22.1 Ϯ 7.2) scored more poorly than con-

trol subjects (mean ϭ 23.8 Ϯ 6.3; p ϭ 0.097) and those

with TTH (mean ϭ 24.5 Ϯ 6.9; p ϭ 0.068) on their School

Certificate exams and achieved significantly lower Sixth

Form Certificate grades (mean ϭ 22.8 Ϯ 9.5) than control

subjects (mean ϭ 26.5 Ϯ 9.8) and those with TTH (mean ϭ

28.5 Ϯ 10.7).

As expected, verbal IQ in childhood was a strong predic-tor of Sixth Form Certificate grades (b ϭ 0.539, t ϭ 19.1,

p Ͻ 0.001), accounting for 40% of the variance in school

performance. For every 4-point difference in verbal IQ, the

model predicts a 2.16 difference in grades, indicating that

the chance of school success was 9.5% less for students

later diagnosed with migraine.

Those with TTH were slightly more likely than those

with migraine to have achieved secondary school qualifica-

tions (84 versus 82%), but this difference was significant

only for men (78 versus 63%; p ϭ 0.02). A greater number

of study members with TTH (26%) and control subjects

(22%) had obtained a bachelor degree by age 26 compared

with those with migraine (18%). Verbal comprehension

during childhood was the strongest predictor of degree sta-tus in migraineurs, with the likelihood of receiving a bach-

elor degree increasing (OR 1.13; 95% CI 1.01 to 1.26) as

comprehension scores on the ITPA increased.

Discussion. We tested the strength and direction of the association between migraine headache and cogni-tive function. Migraineurs had impaired verbal ability versus headache-free control subjects and individualswith TTH, particularly on measures of verbal compre-hension. Migraineurs had normal reading, verbal ex-pression, and mathematical skills.

The subtle verbal deficits exhibited by migraineursmay have impacted upon later achievement. Consis-tent with an earlier study,31 high school grades andexamination scores were significantly lower and fewermigraineurs achieved secondary school qualificationsor degrees. Migraine sufferers also report significantsocial and work-related impairment and earn less thanthose without headache.32

If verbal impairment were a consequence of the

cumulative effects of headache attacks, one wouldexpect that individuals with a longer history of head-ache would perform more poorly than those with ashorter history. In our study, as in others, cognitiveperformance was unrelated to length of headachehistory,10,12,33-34 medication use,12 or severity and du-ration of migraine attack.10,13 Moreover, because mi-graineurs performed significantly more poorly thanthose with TTH on verbal measures at ages 3, 7, 9,11, and 13, the effect does not appear to be attribut-able to the negative influence of headache pain anddiscomfort in general or reduced educational oppor-tunities. Taken together, the findings that verbal

performance remained consistently lower than theother groups at each assessment age, was first iden-tified at the age 3 assessment, and did not declinewith age suggest that verbal performance was notsignificantly influenced by migraine attacks “per se.”

The results make it more likely that migraine and verbal impairment are associated because of ashared risk factor, not because one causes the other.One proposed risk factor to explain the observed re-lation between migraine, left-handedness, and verbaldeficit is related to delayed development of the lefthemisphere in utero.35,36 Anatomically anomalouspatterns of cerebral asymmetry occur more often in

left handers than right handers37-39

and left andmixed handedness was more prevalent among mi-graineurs in the current study. This suggests thatmigraineurs may be at increased risk of anomalouscerebral dominance during neural development withconcomitant problems in later receptive languageacquisition.

Alternatively, subtle verbal dysfunction could re-late to a generalized impairment in selective atten-tion. Migraineurs have trouble adjusting attentionand require more time for automatic processes asshown on tasks such as the “oddball” paradigm,11

regardless of medication use and attack duration.10

Other studies have found that migraine patientsshow both cortical hyperexcitability as well as a lackof habituation to repeated stimuli as measured by visual and auditory event-related potentials in themigraine interval.2,6,11 In contrast, these anomaliesare not observed during the migraine attack.9

Habituation to a stimulus is generally thought tobe one of the most basic forms of learning and alsothought to protect the brain from information over-load.11 As such, it has been suggested that the mi-graine attack is a protective vascular response tothis potential information overload, particularly inthe left hemisphere of the brain where verbal capac-

September (2 of 2) 2002 NEUROLOGY 59 907



ity may be limited.40 Although our findings cannot atpresent confirm or refute either of these explana-tions, the findings do lend support to the idea thatmigraine headaches are of an early, constitutionalorigin.

Acknowledgment

The authors are indebted to Dr. Phil A. Silva, founding director of the study, Air New Zealand, and the study members for theirparticipation and continued support.

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